Indirect effects of ploidy suggest X chromosome dose, not the X:A ratio, signals sex in Drosophila.
In the textbook view, the ratio of X chromosomes to autosome sets, X:A, is the primary signal specifying sexual fate in Drosophila. An alternative idea is that X chromosome number signals sex through the direct actions of several X-encoded signal element (XSE) proteins. In this alternative, the infl...
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Format: | Article |
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Public Library of Science (PLoS)
2007-12-01
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Series: | PLoS Biology |
Online Access: | http://europepmc.org/articles/PMC2222971?pdf=render |
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author | James W Erickson Jerome J Quintero |
author_facet | James W Erickson Jerome J Quintero |
author_sort | James W Erickson |
collection | DOAJ |
description | In the textbook view, the ratio of X chromosomes to autosome sets, X:A, is the primary signal specifying sexual fate in Drosophila. An alternative idea is that X chromosome number signals sex through the direct actions of several X-encoded signal element (XSE) proteins. In this alternative, the influence of autosome dose on X chromosome counting is largely indirect. Haploids (1X;1A), which possess the male number of X chromosomes but the female X:A of 1.0, and triploid intersexes (XX;AAA), which possess a female dose of two X chromosomes and the ambiguous X:A ratio of 0.67, represent critical tests of these hypotheses. To directly address the effects of ploidy in primary sex determination, we compared the responses of the signal target, the female-specific SxlPe promoter of the switch gene Sex-lethal, in haploid, diploid, and triploid embryos. We found that haploids activate SxlPe because an extra precellular nuclear division elevates total X chromosome numbers and XSE levels beyond those in diploid males. Conversely, triploid embryos cellularize one cycle earlier than diploids, causing premature cessation of SxlPe expression. This prevents XX;AAA embryos from fully engaging the autoregulatory mechanism that maintains subsequent Sxl expression, causing them to develop as sexual mosaics. We conclude that the X:A ratio predicts sexual fate, but does not actively specify it. Instead, the instructive X chromosome signal is more appropriately seen as collective XSE dose in the early embryo. Our findings reiterate that correlations between X:A ratios and cell fates in other organisms need not implicate the value of the ratio as an active signal. |
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spelling | doaj.art-c84f54d249d24c0bbf3bda6857689f0c2022-12-21T20:15:16ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852007-12-01512e33210.1371/journal.pbio.0050332Indirect effects of ploidy suggest X chromosome dose, not the X:A ratio, signals sex in Drosophila.James W EricksonJerome J QuinteroIn the textbook view, the ratio of X chromosomes to autosome sets, X:A, is the primary signal specifying sexual fate in Drosophila. An alternative idea is that X chromosome number signals sex through the direct actions of several X-encoded signal element (XSE) proteins. In this alternative, the influence of autosome dose on X chromosome counting is largely indirect. Haploids (1X;1A), which possess the male number of X chromosomes but the female X:A of 1.0, and triploid intersexes (XX;AAA), which possess a female dose of two X chromosomes and the ambiguous X:A ratio of 0.67, represent critical tests of these hypotheses. To directly address the effects of ploidy in primary sex determination, we compared the responses of the signal target, the female-specific SxlPe promoter of the switch gene Sex-lethal, in haploid, diploid, and triploid embryos. We found that haploids activate SxlPe because an extra precellular nuclear division elevates total X chromosome numbers and XSE levels beyond those in diploid males. Conversely, triploid embryos cellularize one cycle earlier than diploids, causing premature cessation of SxlPe expression. This prevents XX;AAA embryos from fully engaging the autoregulatory mechanism that maintains subsequent Sxl expression, causing them to develop as sexual mosaics. We conclude that the X:A ratio predicts sexual fate, but does not actively specify it. Instead, the instructive X chromosome signal is more appropriately seen as collective XSE dose in the early embryo. Our findings reiterate that correlations between X:A ratios and cell fates in other organisms need not implicate the value of the ratio as an active signal.http://europepmc.org/articles/PMC2222971?pdf=render |
spellingShingle | James W Erickson Jerome J Quintero Indirect effects of ploidy suggest X chromosome dose, not the X:A ratio, signals sex in Drosophila. PLoS Biology |
title | Indirect effects of ploidy suggest X chromosome dose, not the X:A ratio, signals sex in Drosophila. |
title_full | Indirect effects of ploidy suggest X chromosome dose, not the X:A ratio, signals sex in Drosophila. |
title_fullStr | Indirect effects of ploidy suggest X chromosome dose, not the X:A ratio, signals sex in Drosophila. |
title_full_unstemmed | Indirect effects of ploidy suggest X chromosome dose, not the X:A ratio, signals sex in Drosophila. |
title_short | Indirect effects of ploidy suggest X chromosome dose, not the X:A ratio, signals sex in Drosophila. |
title_sort | indirect effects of ploidy suggest x chromosome dose not the x a ratio signals sex in drosophila |
url | http://europepmc.org/articles/PMC2222971?pdf=render |
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